Skip to main content
SpringerLink
Log in

Plant phenolics: neglected secondary metabolites in plant stress tolerance

  • Biochemistry & Physiology - Review Article
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Plants endure various biotic and abiotic stressors throughout their lives due to their sessile nature and therefore different stresses such as salinity, heavy metals, temperature (high or low), soil alkalinity or acidity, or pathogenic attack that impact plant growth and development. To combat such menace, plants have evolved in their metabolism, an effective system of secondary metabolites (SMs) such as phenolics that play critical roles in plant's growth and development under normal and stress conditions. Phenolics perform a wide range of functions and bioactivity in plants. These have multiple protection modes ranging from toxicity and light/UV tolerance to signal transduction activities and are one of the most abundant and diverse classes of SMs found across the plant kingdom. Although phenolic compounds have little involvement in plant growth, they are important in how plants interact with their environment. The metabolic engineering of genes related to phenylpropanoid and flavonoid pathways responsible for phenolics biosynthesis has attracted a lot of attention in biotechnology and plant science for securing stress resistance in crop plants. This review discusses how phenolic compounds interact in plants under harsh environmental conditions and provides a current and updated research related to phenolics with a focus on improving plant stress tolerance to achieve food security in agriculture. Alteration in phenolics could potentially impact feed, fodder, and fuel for the coming generation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Data were available upon request from the corresponding author.

References

  • Abu ESW, Hegab MM, Abd EH, Zinta G, Asard H (2013) Ability of ellagic acid to alleviate osmotic stress on chickpea seedlings. Plant Physiol Biochem 71:173–183

    Article  Google Scholar 

  • Ahmed NU, Park JI, Jung HJ, Hur Y, Nou IS (2015) Anthocyanin biosynthesis for cold and freezing stress tolerance and desirable color in Brassica rapa. Func Integ Genom 15:383–394

    Article  CAS  Google Scholar 

  • Ahuja I, Kissen R, Bones AM (2012) Phytoalexins in defense against pathogens. Trends Plant Sci 17:73–90

    Article  CAS  PubMed  Google Scholar 

  • Albert A, Sareedenchai V, Heller W, Seidlitz HK, Zidorn C (2009) Temperature is the key to altitudinal variation of phenolics in alpine plants. Oecologia 160:1–8

    Article  PubMed  Google Scholar 

  • Ali RM, Abbas HM (2003) Response of salt stressed barley seedlings to phenylurea. Plant Soil and Environ 49:158–162

    Article  Google Scholar 

  • Anosheh HP, Emam Y, Ashraf M, Foolad MR (2012) Exogenous application of salicylic acid and chlormequat chloride alleviates negative effects of drought stress in wheat. AdvStudBiol 4:501–520

    Google Scholar 

  • Antognoni F, Zheng S, Pagnucco C, Baraldi R, Poli F, Biondi S (2007) Induction of flavonoid production by UV-B radiation in Passiflora quadrangularis callus cultures. Fitoterapia 78:345–352

    Article  CAS  PubMed  Google Scholar 

  • Araujo L, Wilka MSB, Jonas AR, Sergio AF, Fabricio AR (2016) Alkaloids and phenolics biosynthesis increases mango resistance to infection by Ceratocystis fimbriata. Bragantia 75:199–211

    Article  CAS  Google Scholar 

  • Arbona V, Manzi M, de Ollas C, Gómez CA (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int J Mol Sci 14:4885–4811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee S, Sen R, Pandey RA, Chakrabarti T, Satpute D, Giri BS, Mudliar S (2009) Evaluation of wet air oxidation as a pretreatment strategy for bioethanol production from rice husk and process optimization. Biomass Bioener 33:1680–1686

    Article  CAS  Google Scholar 

  • Baskar V, Venkatesh R, Ramalingam S (2018) Flavonoids (antioxidants systems) in higher plants and their response to stresses. Antioxidants and antioxidant enzymes in higher plants. Springer, pp 253–268

    Chapter  Google Scholar 

  • Belkhadi A, Hediji H, Abbes Z, Nouairi I, Barhoumi Z, Zarrouk M, Chaibi W, Djebali W (2010) Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linumusitatissimum L. Ecotoxicol Environ Saf 73:1004–1011

    Article  CAS  PubMed  Google Scholar 

  • Bentivenha JP, Canassa VF, Baldin EL, Borguini MG, Lima GP, Lourenção AL (2018) Role of the rutin and genistein flavonoids in soybean resistance to Piezodorusguildinii (Hemiptera: Pentatomidae). Arthropod Plant Interact 12:311–320

    Article  Google Scholar 

  • Bernáth J, Tetenyi P (1979) The effect of environmental factors on growth. development and alkaloid production of poppy (Papaver somniferum L.): I. Responses to day-length and light intensity. Biochem Physiol Der Pflan 174:468–478

    Article  Google Scholar 

  • Bi JL, Murphy JB, Felton GW (1997) Does salicylic acid act as a signal in cotton for induced resistance to Helicoverpazea. J Chem Ecol 23:1805–1818

    Article  CAS  Google Scholar 

  • Bortesi L, Fischer R (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52

    Article  CAS  PubMed  Google Scholar 

  • Bota C, Deliu C (2011) The effect of copper sulphate on the production of flavonoids in Digitalis lanata cell cultures. Farmacia 59:113–118

    CAS  Google Scholar 

  • Bourgaud F, Gravot A, Milesi S, Gontier E (2001) Production of plant secondary metabolites: a historical perspective. Plant Sci 161:839–851

    Article  CAS  Google Scholar 

  • Broeckling CD, Huhman DV, Farag MA, Smith JT, May GD, Mendes P, Dixon RA, Sumner LW (2005) Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism. J Exp Bot 56:323–336

    Article  CAS  PubMed  Google Scholar 

  • Budovská M, Pilátová M, Varinská L, Mojžiš J, Mezencev, (2013) The synthesis and anticancer activity of analogs of the indole phytoalexins brassini 1-methoxyspirobrassinol methyl ether and cyclobrassinin. Bioorg Med Chem 21:6623–6633

    Article  PubMed  Google Scholar 

  • Çakir R, Çebi U (2010) The effect of irrigation scheduling and water stress on the maturity and chemical composition of Virginia tobacco leaf. Field Crops Res, 119(2-3), 269-276

    Article  Google Scholar 

  • Chalker SL, Fnchigami LH (1989) The role of phenolic compounds in plant stress responses. In: Paul HL (ed) Low temperature stress physiology in crops. CRC Press Inc., p 40

    Google Scholar 

  • Chan L, Koay S, Boey P, Bhatt A (2010) Effects of abiotic stress on biomass and anthocyanin production in cell cultures of Melastomamalabathricum. Biol Res 43:127–135

    Article  CAS  PubMed  Google Scholar 

  • Chavoushi M, Najafi F, Salimi A, Angaji SA (2019) Improvement in drought stress tolerance of safflower during vegetative growth by exogenous application of salicylic acid and sodium nitroprusside. Ind Crops Prod 134:168–176

    Article  CAS  Google Scholar 

  • Chen F, Dixon R (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Guo Q, Liu L, Liao L, Zaibiao Z (2011) Influence of fertilization and drought stress on the growth and production of secondary metabolites in Prunella vulgaris L. J Med Plants Res 5:1749–1755

    CAS  Google Scholar 

  • Chen S, Wu F, Li Y, Qian Y, Pan X, Li F, Wang Y, Wu Z, Fu C, Lin H, Yang A (2019) NtMYB4 and NtCHS1 are critical factors in the regulation of flavonoid biosynthesis and are involved in salinity responsiveness. Front Plant Sci 10:178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng GX, Li RJ, Wang M, Huang LJ, Khan A, Ali M, Gong ZH (2018) Variation in leaf color and combine effect of pigments on physiology and resistance to whitefly of pepper (Capsicum annuum L.). Sci Horti 229:215–225

    Article  CAS  Google Scholar 

  • Chishaki N, Horiguchi T (1997) Responses of secondary metabolism in plants to nutrient deficiency. Soil Sci Plant Nutr 43:987–991

    Article  CAS  Google Scholar 

  • Cho Y, Njitiv N, Chen X, Lightfood DA, Wood AJ (2003) Trigonelline concentration in field-grown soybean in response to irrigation. Biol Plant 46:405–410

    Article  CAS  Google Scholar 

  • Christie PJ, Alfenito MR, Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194:541–549

    Article  CAS  Google Scholar 

  • Chutipaijit S, Cha-um S, Sompornpailin K (2011) High contents of proline and anthocyanin increase protective response to salinity in ‘Oryza sativa’Lspp’.indica’. Aus J Crop Sci 5:1191–1198

    CAS  Google Scholar 

  • Cirillo V, D’Amelia V, Esposito M, Amitrano C, Carillo P, Carputo D, Maggio A (2021) Anthocyanins are key regulators of drought stress tolerance in Tobacco. Biol 10:139

    Article  CAS  Google Scholar 

  • Colling J, Groenewald JH, Makunga NP (2010) Genetic alterations for increased coumarin production lead to metabolic changes in the medicinally important Pelargonium sidoides DC (Geraniaceae). Metab Eng 12:561–572

    Article  CAS  PubMed  Google Scholar 

  • Consortium TTG (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

  • Constabel CP, Yoshida K, Walker V (2014) Diverse ecological roles of plant tannins: plant defense and beyond. Recent Adv Pol Res 4:115–142

    Article  CAS  Google Scholar 

  • Cotas J, Leandro A, Adriana M, Pedro P, Diana F, Artur G, Ana S, Gabriela P, Leonel (2020) Marine drugs seaweed phenolics: from extraction to applications. Mar Drugs 18:384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cote J, Caillet S, Doyon G, Sylvain JE, Lacroix M (2010) Analyzing cranberry bioactive compounds. Crit Rev Food Sci Nutr 50:872–888

    Article  CAS  PubMed  Google Scholar 

  • Cowan M (1999) Plant products as antimicrobial agents. Clin Microbial Rev 12:564–582

    Article  CAS  Google Scholar 

  • Darvill AG, Albersheim P (1984) Phytoalexins and their elicitors—a defence against microbial infection in plants. Ann Rev Plant Physiol 35:243–275

    Article  CAS  Google Scholar 

  • Dawid C, Hille K (2018) Functional metabolomics—a useful tool to characterize stress-induced metabolome alterations opening new avenues towards tailoring food crop quality. Agronomy 8:138

    Article  CAS  Google Scholar 

  • De Abreu IN, Mazzafera P (2005) Effect of water and temperature stress on the content of active constituents of Hypericum brasiliense Choisy. Plant Physiol Biochem 43:241–248

    Article  Google Scholar 

  • Délano FJP, Avilés AH, Casarrubias CK, Casique AG, Castrillón APA, Herrera EL, Massange SJ, Martínez GNA, Parra-Cota FI, Vargas OE (2011) Transcriptomic analysis of grain amaranth (Amaranthus hypochondriacus) using 454 pyrosequencing: Comparison with A. tuberculatus, expression profiling in stems and in response to biotic and abiotic stress. BMC Genom 12:363

    Article  Google Scholar 

  • Dhakshinamoorthy S, Mariama K, Elsen A, De Waele D (2014) Phenols and lignin are involved in the defence response of banana (Musa) plants to Radopholussimilis infection. Int J Nematol 16:565–576

    Article  CAS  Google Scholar 

  • Dushnicky LG, Ballance GM, Sumner MJ, MacGregor AW (1998) The role of lignification as a resistance mechanism in wheat to a toxin-producing isolate of Pyrenophoratritici-repentis. Can J Plant Pathol 20:35–47

    Article  Google Scholar 

  • Edreva AM, Velikova V, Tsonev T (2000) Phenylamides in plants. Russ J Plant Physiol 54:287–301

    Article  Google Scholar 

  • Ejike CECC, Gong M, Udenigwe CC (2013) Phytoalexins from the Poaceae: Biosynthesis function and prospects in food preservation. Food Res Int 52:167–177

    Article  CAS  Google Scholar 

  • Erb M, Kliebenstein DJ (2020) Plant secondary metabolites as defenses, regulators, and primary metabolites: the blurred functional trichotomy. Plant Physiol 184:39–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan X, Fan B, Wang Y, Yang W (2016) Anthocyanin accumulation enhanced in Lc-transgenic cotton under light and increased resistance to bollworm. Plant Biotechnol Rep 10:1–11

    Article  PubMed  Google Scholar 

  • Fraser CM, Chapple C (2011) The phenylpropanoid pathway in Arabidopsis. Arab Book 9:0152

    Article  Google Scholar 

  • Fu R, Shi M, Deng C, Zhang Y, Zhang X, Wang Y, Kai G (2020) Improved phenolic acid content and bioactivities of Salvia miltiorrhiza hairy roots by genetic manipulation of RAS and CYP98A14. Food Chem 331:127365

    Article  CAS  PubMed  Google Scholar 

  • Fucile G, Falconer S, Christendat D (2008) Evolutionary diversification of plant shikimate kinase gene duplicates. PloS Genet 4:1000292

    Article  Google Scholar 

  • Furlan CM, Motta LB, Santos DYAC, Petridis GK (2011) Tannins: What do they represent in plant life. Tannins types, foods containing and nutrition. Nova Science Publishers, New York

    Google Scholar 

  • Gandikota M, de Kochko A, Chen L, Ithal N, Fauquet C, Reddy AR (2001) Development of transgenic rice plants expressing maize anthocyanin genes and increased blast resistance. Mol Plant Breed 7:73–83

    Article  CAS  Google Scholar 

  • Gay PA, Tuzun S (2000) Involvement of a novel peroxidase isozyme and lignification in hydathodes in resistance to black rot disease in cabbage. Canad J Bot 78:1144–1149

    Article  CAS  Google Scholar 

  • Gray DE, Pallardy SG, Garrett HE, Rottinghaus G (2003) Acute drought stress and plant age effects on alkamide and phenolic acid content in purple coneflower roots. Planta Med 69:50–55

    Article  CAS  PubMed  Google Scholar 

  • Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405

    Article  CAS  PubMed  Google Scholar 

  • Grindberg RV, IshoeyT BD, Esquenazi E, Coates R, Wei-Ting L, Gerwick WH (2011) Single cell genome amplification accelerates identification of the apratoxin biosynthetic pathway from a complex microbial assemblage. PLoS ONE 6:1–12

    Article  Google Scholar 

  • Grindberg RV, Shuman CF, Sorrels CM,Wingerd J,Gerwick WH (2007) Neurotoxic alkaloids from cyanobacteria. In: Fattorusso E (Ed) Modern alkaloids pp 139–170

  • Gu H, Wang Y, Xie H, Qiu C, Zhang S, Xiao J, Li H, Chen L, Li X, Ding Z (2020) Drought stress triggers proteomic changes involving lignin, flavonoids and fatty acids in tea plants. Sci Rep 10:1–11

    Article  Google Scholar 

  • Halpin C, Knight ME, Foxon GA, Campbell MM, Boudet AM, Boon JJ, Chabbert B, Tollier MT, Schuch W (1994) Manipulation of lignin quality by downregulation of cinnamyl alcohol dehydrogenase. Plant J 6:339–350

    Article  CAS  Google Scholar 

  • Halvorson JJ, Gonzalez JM, Hagerman AE, Smith JL (2009) Sorption of tannin and related phenolic compounds and effects on soluble-N in soil. Soil Biol Biochem 41:2002–2010

    Article  CAS  Google Scholar 

  • Hanson D, Sharkey TD (2001) Effect of growth conditions on isoprene emission and other thermotolerance-enhancing compounds. Plant Cell Environ 24:929–936

    Article  CAS  Google Scholar 

  • Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochem Lett 68:2831–2846

    Article  CAS  Google Scholar 

  • Hassan A (2012) Effects of mineral nutrients on physiological and biochemical processes related to secondary metabolites production in medicinal herbs. Med Arom Plant Sci Biotechnol 6:105–110

    Google Scholar 

  • Hernandez I, Alegre L, Munne BS (2006) Enhanced oxidation of flavan-3-ols and proanthocyanidin accumulation in water-stressed tea plants. Phytochem Lett 67:1120–1126

    Article  CAS  Google Scholar 

  • Higuchi M (2014) Antioxidant properties of wheat bran against oxidative stress. Wheat and rice in disease prevention and health. Academic Press, pp 181–199

    Chapter  Google Scholar 

  • Hipskind J, Wood K, Nicholson RL (1996) Localized stimulation of anthocyanin accumulation and delineation of pathogen ingress in maize genetically resistant to Bipolarismaydisrace O. Physiol Mol Plant Pathol 49:247–256

    Article  CAS  Google Scholar 

  • Homoki JR, Nemes A, Fazekas E, Gyémánt G, Balogh P, Gál F, Remenyik J (2016) Anthocyanin composition antioxidant efficiency and α-amylase inhibitor activity of different hungarian sour cherry varieties (Prunus cerasus L.). Food Chem 194:222–229

    Article  CAS  PubMed  Google Scholar 

  • Huang WK, Ji HL, Gheysen G, Kyndt T (2016) Thiamine-induced priming against root-knot nematode infection in rice involves lignification and hydrogen peroxide generation. Mol Plant Pathol 17:614–624

    Article  CAS  PubMed  Google Scholar 

  • Hussain S, Fareed S, Ansari S, Rahman A, Iffat ZA, Saeed M (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioall Sci 4:10–20

    Article  Google Scholar 

  • Ibrahim MM, Zawawy EWK, Abdel FYR, Soliman NA, Agblevor FA (2011) Comparison of alkaline pulping with steam explosion for glucose production from rice straw. Carbohyd Poly 83:720–726

    Article  CAS  Google Scholar 

  • Isah T (2019) Stress and defense responses in plant secondary metabolites production. Biol Res 52:39

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaafar HZ, Ibrahim MH, Fakri NFM (2012) Impact of soil field water capacity on secondary metabolites, phenylalanine ammonia-lyase (PAL), malondialdehyde (MDA) and photosynthetic responses of Malaysian kacipfatimah (Labisia pumila Benth). Molecules 17:7305–7322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jamalian S, Gholami M, Ashari ME (2013) Abscisic acid-mediated leaf phenolic compounds, plant growth and yield is strawberry under different salt stress regimes. Theor Exp Plant Physiol 25:291–299

    Google Scholar 

  • Jamloki A, Malini BMC, Nautiyal BP (2021) Elucidating the relevance of high temperature and elevated CO2 in plant secondary metabolites (PSMs) production. Heliyon 7:8

    Article  Google Scholar 

  • Jan R, Asaf S, Numan M, Lubna KKM (2021) Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy 11:968

    Article  CAS  Google Scholar 

  • Jansen G, Jürgens HU, Ordon F (2009) Effects of temperature on the alkaloid content of seeds of Lupinus angustifolius cultivars. J Agric Crop Sci 195:172–177

    Article  CAS  Google Scholar 

  • Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2013) Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. J Exp Bot 64:2255–2268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones ME, Kossel A (1953) A biographical sketch. Yale J Biol Med 26:80–97

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jung W, Yu O, Lau SMC, O’Keefe DP, OdellJ FG, Gonigle BM (2000) Identification and expression of isoflavone synthase, the key enzyme for biosynthesis of isoflavones in legumes. Nat Biotechnol 18:208–212

    Article  CAS  PubMed  Google Scholar 

  • Kabiri R, Nasibi F, Farahbakhsh H (2014) Effect of exogenous salicylic acid on some physiological parameters and alleviation of drought stress in Nigella sativa plant under hydroponic culture. Plant Prot Sci 50:43–51

    Article  Google Scholar 

  • Kangatharalingam N, Pierce ML, Bayles MB, Essenberg M (2002) Epidermal anthocyanin production as an indicator of bacterial blight resistance in cotton. Physiol Mol Plant Pathol 61:189–195

    Article  CAS  Google Scholar 

  • Kariyat RR, GaffoorI SS, Dixon CW, Frock N, Moen J, Moraes DCM, Mescher MC, Thompson GA, Chopra S (2019) Sorghum 3-deoxyanthocyanidin flavonoids confer resistance against corn leaf aphid. J Chem Ecol 45:502–514

    Article  CAS  PubMed  Google Scholar 

  • Kennedy DO, Wightman EL (2011) Herbal extracts and phytochemicals: plant secondary metabolites and the enhancement of human brain function. Adv Nutr 2:32–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kidd PS, Llugany M, Poschenrieder C, Gunsé B, Barceló J (2001) The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J Exp Bot 52:1339–1352

    CAS  PubMed  Google Scholar 

  • Kirk H, Vrieling K, vander ME, Klinkhamer PGL, (2010) Species by environment interactions affect pyrrolizidine alkaloid expression in Senecio jacobaea, Senecio aquaticus, and their hybrids. J ChemEcol 36:378–387

    CAS  Google Scholar 

  • Koike N, Hyakumachi M, Kageyama K, Tsuyumu S, Doke N (2001) Induction of systemic resistance in cucumber against several diseases by plant growth-promoting fungi: lignification and superoxide generation. Eur J Plant Pathol 107:523–533

    Article  CAS  Google Scholar 

  • Kootstra AMJ, Beeftink HH, Scott EL, Sanders JP (2009) Comparison of dilute mineral and organic acid pretreatment for enzymatic hydrolysis of wheat straw. Biochem Eng J 46:126–131

    Article  CAS  Google Scholar 

  • Kostyn K, Szatkowski M, Kulma A, Kosieradzka I, Szopa J (2013) Transgenic potato plants with overexpression of dihydroflavonol reductase can serve as efficient nutrition sources. J Agr Food Chem 61:6743–6753

    Article  CAS  Google Scholar 

  • Kostyuk VA, Potapovich AI, Strigunova EN, Kostyuk TV, Afanas’ev IB (2004) Experimental evidence that flavonoid metal complexes may act as mimics of superoxide dismutase. Arch BiochemBiophys 428:204–208

    Article  CAS  Google Scholar 

  • Kovach A, Wegrzyn JL, Parra G, Holt C, Bruening GE (2010) The Pinus taeda genome is characterized by diverse and highly diverged repetitive sequences. BMC Gen 11:420

    Article  Google Scholar 

  • Krzyzanowska J, CzubackaA O, W, (2010) Dietary phytochemicals and human health. In: Giardi MT, Rea G, Berra B (eds) Bio-Farms for nutraceuticals: functional food and safety control by biosensors. Springer, pp 74–99

    Chapter  Google Scholar 

  • Kubota N, Mimura H, Shimamura K (1988) The effects of drought and flooding on the phenolic compounds in peach fruits. Sci Rep Fac Agr 171:17–21

    Google Scholar 

  • Lattanzio V, Lattanzio VMT, Cardinali A (2006) Role of phenolic in the resistance mechanisms of plants against fungal pathogens and insects. Phytochem Adv Res 661:23–67

    Google Scholar 

  • Lattanzio V, Kroon PA, Quidea S,Treutter D (2008) Plant phenolics—secondary metabolites with diverse functions. Recent Advan Polyp Res 1–35

  • Le Gall G, DuPont MS, Mellon FA, Davis AL, Collins GJ, Verhoeyen ME, Colquhoun IJ (2003) Characterization and content of flavonoid glycosides in genetically modified tomato (Lycopersicon esculentum) fruits. J Agric Food Chem 51:2438–2446

    Article  PubMed  Google Scholar 

  • Lee SK, Kim WS (2015) Floral pigmentation and expression of anthocyanin-related genes in bicolored roses’ pinky girl’as affected by temporal heat stress. Hortic Sci Technol 33:923–931

    CAS  Google Scholar 

  • Li Q, Yu Gao Y, Dai AH, Bai JG (2011) Cinnamic acid pretreatment mitigates chilling stress of cucumber leaves through altering antioxidant enzyme activity. J Plant Physiol 168:927–934

    Article  CAS  PubMed  Google Scholar 

  • Li X, Mupondwa E, Panigrahi S, Tabil L, Sokhansanj S, Stumborg MA (2012) Review of agricultural crop residue supply in Canada for cellulosic ethanol production. Ren Sus Energ Rev 16:2954–2965

    Article  CAS  Google Scholar 

  • Li P, Li YJ, Zhang FJ, Zhang GZ, Jiang XY, Yu HM, Hou BK (2017) The Arabidopsis UDP-glycosyltransferases UGT79B2 and UGT79B3, contribute to cold, salt and drought stress tolerance via modulating anthocyanin accumulation. The Plant J 89:85–103

    Article  CAS  PubMed  Google Scholar 

  • Liakopoulos G, Karabourniotis G (2005) Boron deficiency and concentrations and composition of phenolic compounds in Olea europaea leaves: a combined growth chamber and field study. Tree Physiol 25:307–315

    Article  CAS  PubMed  Google Scholar 

  • Lim JH, Park KJ, Kim BK, Jeong JW, Kim HJ (2012) Effect of salinity stress on phenolic compounds and carotenoids in buckwheat (Fagopyrum esculentum M.) sprout. Food Chem 135:1065–1070

    Article  CAS  PubMed  Google Scholar 

  • Limayem A, Ricke SC (2012) Lignocellulosic biomass for bioethanol production: current perspectives, potential issues and future prospects. Prog Energy Comb Sci 38:449–467

    Article  CAS  Google Scholar 

  • Lin Y, Qasim M, Hussain M, Akutse KS, Avery PB, Dash CK, Wang L (2017) The herbivore-induced plant volatiles methyl salicylate and menthol positively affect growth and pathogenicity of entomopathogenic fungi. Sci Rep 7:40494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z (2000) Drought-induced in vivo synthesis of camptothecin in Camptotheca acuminata seedlings. Physiol Plant 110:483–488

    CAS  Google Scholar 

  • Liu Q, Zheng L, He F, Zhao FJ, Shen Z, Zheng L (2015) Transcriptional and physiological analyses identify a regulatory role for hydrogen peroxide in the lignin biosynthesis of copper-stressed rice roots. Plant Soil 387:323–336

    Article  CAS  Google Scholar 

  • Liu W, Zhang Y, Yuan X, Xuan Y, Gao Y, Yan Y (2016) Exogenous salicylic acid improves salinity tolerance of Nitrariatangutorum. Russ J Plant Physiol 63:132–142

    Article  CAS  Google Scholar 

  • Liu R, Ding LN, Li M, Cao W, Wang YK, Wang WJ, Yu YK, Wang Z, Zhu KM, Tan XL (2020) Characterization of a rapeseed anthocyanin-more mutant with enhanced resistance to Sclerotinia sclerotiorum. J Plant Growth Regul 39:703–716

    Article  CAS  Google Scholar 

  • Long L, Liu J, Gao Y, Xu FC, Zhao JR, Li B, Gao W (2019) Flavonoid accumulation in spontaneous cotton mutant results in red coloration and enhanced disease resistance. Plant Physiol Biochem 143:40–49

    Article  CAS  PubMed  Google Scholar 

  • Lorenc KK, Jafra S, Oszmiański J, Szopa J (2005) Ectopic expression of anthocyanin 5-O-glucosyltransferase in potato tuber causes increased resistance to bacteria. J Agric Food Chem 53:272–281

    Article  Google Scholar 

  • Lu Y, Chen Q, Bu Y, Luo R, Hao S, Zhang J, Tian J, Yao Y (2017) Flavonoid accumulation plays an important role in the rust resistance of Malus plant leaves. Front Plant Sci 8:1286

    Article  PubMed  PubMed Central  Google Scholar 

  • Macoy DM, Kim WY, Lee SY, Kim MG (2015) Biotic stress related functions of hydroxycinnamic acid amide in plants. J Plant Biol 58:156–163

    Article  CAS  Google Scholar 

  • Madeira JJV, Teixeira CB, Macedo GA (2015) Biotransformation and bioconversion of phenolic compounds obtainment: an overview. Crit Rev Biotechnol 35:75–81

    Article  Google Scholar 

  • Makowski W, Królicka A, Nowicka A, Zwyrtková J, Tokarz B, Pecinka A, Banasiuk R, Tokarz KM (2021) Transformed tissue of Dionaea muscipula J. Ellis as a source of biologically active phenolic compounds with bactericidal properties. Appl Microbiol Biotechnol 105:1215–1226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mathesius U (2018) Flavonoid functions in plants and their interactions with other organisms. Plants 7:30

    Article  PubMed  PubMed Central  Google Scholar 

  • Mayer KF, Waugh R, Brown JW, Schulman A, Langridge P, Platzer M, Fincher GB, Muehlbauer GJ, Sato K, Close TJ, Wise RP, Stein N (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 29:711–716

    Google Scholar 

  • Melillo MT, Bleve-Zacheo T, Zacheo G (1993) Rapid lignin biosynthesis in pea roots infected with Heteroderagoettingiana. Plant Biosyst 127:1202–1204

    Google Scholar 

  • Minh LT, Khang DT, Thu Ha PT (2016) Effects of salinity stress on growth and phenolics of Rice (Oryza sativa L.). Int Lett Nat Sci 57:1–10

    Google Scholar 

  • Mira L, Fernandez MT, Santos M, Rocha R, Florêncio MH, Jennings KR (2002) Interactions of flavonoids with iron and copper ions: a mechanism for their antioxidant activity. Free Rad Res 36:1199–1208

    Article  CAS  Google Scholar 

  • Mkhize T, Mthembu LD, Gupta R, Kaur A, Kuhad RC, Reddy P, Deenadayalu N (2015) Enzymatic saccharification of acid/alkali pre-treated, mill-run, and depithed sugarcane bagasse. Biores 11:6267–6285

    Google Scholar 

  • Moerschbacher BM, Noll U, Ocampo CA, FlottBE GotthardtU, WüslefeldA RHJ (1990) Hypersensitive lignification response as the mechanism of non-host resistance of wheat against oat crown rust. Physiol Plant 78:609–615

    Article  CAS  Google Scholar 

  • Moura JCMS, Bonine CAV, Viana JDOF, DornelasMC MP (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integ Plant Biol 52:360–376

    Article  CAS  Google Scholar 

  • Mousavi A, Pourakbar L, Moghaddam SS, Popović-Djordjević J (2021) The effect of the exogenous application of EDTA and maleic acid on tolerance, phenolic compounds, and cadmium phytoremediation by okra (Abelmoschus esculentus L.) exposed to Cd stress. J Environ Chem Eng 9:105456

    Article  CAS  Google Scholar 

  • Mrid RB, Benmrid B, Hafsa J, Boukcim H, Sobeh M, Yasri A (2021) Secondary metabolites as biostimulant and bioprotectant agents: a review. Sci Total Environ 777:146204

    Article  Google Scholar 

  • Muszynska B, Ekiert H, Kwiecien I, MaslankaA ZR, Beerhues L (2014) Comparative analysis of therapeutically important indole compounds in in vitro cultures of Hypericum perforatum cultivars by HPLC and TLC analysis coupled with densitometric detection. Nat Prod Commun 9:1437–1430

    CAS  PubMed  Google Scholar 

  • Naing AH, Kim CK (2021) Abiotic stress-induced anthocyanins in plants: their role in tolerance to abiotic stresses. Physiol Plant 172:1711–1723

    Article  CAS  PubMed  Google Scholar 

  • Nielsen E, Temporiti MEE, Cella R (2019) Improvement of phytochemical production by plant cells and organ culture and by genetic engineering. Plant Cell Rep 38:1199–1215

    Article  CAS  PubMed  Google Scholar 

  • Nik K, Gilbert K, Alexandra C (2018) Abiotic stresses induce different localizations of anthocyanins in Arabidopsis. Plant Signal Behav 10:1027850

    Google Scholar 

  • Obaid N, Kortschot MT, Sain M (2016) Lignin-based foaming materials lignin. Polymer composite. Elsevier, pp 217–232

    Google Scholar 

  • Oh JY, Kim YJ, Jang MG, Joo SC, Kwon WS, Kim SY, Yang DC (2014) Investigation of ginsenosides in different tissues after elicitor treatment in Panax ginseng. J Ginseng Res 38:270–277

    Article  PubMed  PubMed Central  Google Scholar 

  • Othman L, Sleiman A, Abdel MRM (2019) Antimicrobial activity of polyphenols and alkaloids in middle eastern plants. Front Microbiol 10:911

    Article  PubMed  PubMed Central  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  PubMed  Google Scholar 

  • Park CH, Xu H, Yeo HJ, Park YE, Hwang GS, Park NI, Park SU (2021) Enhancement of the flavone contents of Scutellaria baicalensis hairy roots via metabolic engineering using maize Lc and Arabidopsis PAP1 transcription factors. Metab Eng 64:64–73

    Article  CAS  PubMed  Google Scholar 

  • Parsaeimehr A, Sargsyan E, Vardanyan A (2011) Expression of secondary metabolites in plants and their useful perspective in animal health. ABAH Bioflux 3:115–124

    CAS  Google Scholar 

  • Parvin K, Nahar K, Hasanuzzaman M, Bhuyan MB, Mohsin SM, Fujita M (2020) Exogenous vanillic acid enhances salt tolerance of tomato: Insight into plant antioxidant defense and glyoxalase systems. Plant Physiol Biochem 150:109–120

    Article  CAS  PubMed  Google Scholar 

  • Peterhansel C, Niessen M, Rashad M, Kebeish (2008) Metabolic engineering towards the enhancement of photosynthesis. Photochem Photobiol 84:1317–1323

    Article  CAS  PubMed  Google Scholar 

  • Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T (2009) Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem 47:224–231

    Article  CAS  PubMed  Google Scholar 

  • Pott DM, Osorio S, Vallarino JG (2019) From central to specialized metabolism: an overview of some secondary compounds derived from the primary metabolism for their role in conferring nutritional and organoleptic characteristics to fruit. Front Plant Sci 10:835

    Article  PubMed  PubMed Central  Google Scholar 

  • Project IRGS (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Qiang Z, Thomsen AB (2012) Effect of different wet oxidation pretreatment conditions on ethanol fermentation from corn stover. Front Plant Sci 53:958

    Google Scholar 

  • Rabelo SC, MacielFilho R, Costa AC (2009) Lime pretreatment of sugarcane bagasse for bioethanol production. Appl Biochem Biotechnol 153:139–150

    Article  CAS  PubMed  Google Scholar 

  • Ramani S, Jayabaskaran C (2008) Enhanced catharanthine and vindoline production in suspension cultures of Catharanthus roseus by ultraviolet-B light. J Mol Signal 3:1–6

    Article  Google Scholar 

  • Ramirez EK, Vidal LH, Hidalgo D, Moyano E, Golenioswki M, Cusidó RM, Palazon J (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21:182

    Article  Google Scholar 

  • Rangasamy M (2007) Role of leaf sheath toughness, lignification and anatomy in resistance of St. Augustinegrasses against southern chinch bug, Blissusinsualris Barber (Hemiptera: Blissidae). J Econ Entomol 102:432–439

    Article  Google Scholar 

  • Rangasamy M, Rathinasabapathi B, McAuslane HJ, Cherry RH, Nagata RT (2009) Role of leaf sheath lignification and anatomy in resistance against southern chinch bug (Hemiptera: Blissidae) in St. Augustinegrass. J Econ Entomol 102:432–439

    Article  PubMed  Google Scholar 

  • Rao MJ, Xu Y, Tang X, Huang Y, Liu J, Deng X, Xu Q (2020) CsCYT75B1, a citrus cytochrome P450 gene, is involved in accumulation of antioxidant flavonoids and induces drought tolerance in transgenic Arabidopsis. Antioxidants 9:161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raza A, Razzaq A, Mehmood SS, Zou X, Zhang X, Lv Y, Xu J (2009) Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8:34

    Article  Google Scholar 

  • Rea G, Antonacci A, Lambreva M, Margonelli A, Ambrosi C, Giardi MT (2010) The nutrasnacks project: basic research and biotechnological programs on nutraceutical. In: Giardi MT, Rea G, Berra B (eds) Bio-farms for nutraceuticals: functional food and safety control by biosensors. Springer, US

    Google Scholar 

  • Regvar M, Bukovnik U, Likar M, Kreft I (2012) UV-B radiation affects flavonoids and fungal colonization in Fagopyrum esculentum and F. tataricum. Cent Eur J Biol 7:275–283

    CAS  Google Scholar 

  • Rehman A, Farooq M, Naveed M, Ozturk L, Nawaz A (2018) Pseudomonas-aided zinc application improves the productivity and biofortification of bread wheat. Crop past Sci 69:659–672

    Article  CAS  Google Scholar 

  • Riaz U, Kharal MA, Murtaza G, Zaman UQ, Javaid S, Malik HA, Aziz H, Abbas Z (2019) Prospective roles and mechanisms of caffeic acid in counter plant stress: a mini review. Pak J Agr Sci 32:8

    Google Scholar 

  • Robbins MP, Paolocci F, HughesJW TV, Allison G, Arcioni S, Morris P, Damiani F (2003) Sn, a maize bHLH gene, modulates anthocyanin and condensed tannin pathways in Lotus corniculatus. J Exp Bot 54:239–248

    Article  CAS  PubMed  Google Scholar 

  • Rosenfeld HJ, Aaby K, Lea P (2002) Influence of temperature and plant density on sensory quality and volatile terpenoids of carrot (Daucus carota L.) root. J Sci Food Agr 82:1384–1390

    Article  CAS  Google Scholar 

  • Ryan KG, Swinny EE, Winefield C, Markham KR (2001) Flavonoids and UV photoprotection in Arabidopsis mutants. Z Nat C 56:745–754

    CAS  Google Scholar 

  • Sabella E, Luvisi A, Aprile A, Negro C, Vergne M, Nicolì F, Miceli A, De Bellis L (2018) Xylella fastidiosa induces differential expression of lignification related-genes and lignin accumulation in tolerant olive trees cv Leccino. J Plant Physiol 220:60–68

    Article  CAS  PubMed  Google Scholar 

  • Saheb DN, Jog JP (1999) Natural fiber polymer composites: a review. Adv Poly Sci 18:351–363

    CAS  Google Scholar 

  • Salama ZA, Gaffar AA, Mohamed MEF (2015) Genotypic variations in phenolic, flavonoids an their antioxidant activities in maize plants treated with Zn (II) HEDTA grown in salinized media. Indian J Agric Sci 6:397–405

    Google Scholar 

  • Saleh AM, Madany MMY (2015) Coumarin pretreatment alleviates salinity stress in wheat seedlings. Plant Physiol Biochem 88:27–35

    Article  CAS  PubMed  Google Scholar 

  • Šamec D, Karalija E, Šola I, Vujčić Bok V, Salopek SB (2021) The role of polyphenols in abiotic stress response: the influence of molecular structure. Plants 10:118

    Article  PubMed  PubMed Central  Google Scholar 

  • Schijlen CH, Ric DV, Harry J, Hetty VB, Jos M, Arjen VT, Stefan M, Arnaud B (2006) Pathway engineering for healthy phytochemicals leading to the production of novel flavonoids in tomato fruit. Plant Biotechnol J 4:433–444

    Article  CAS  PubMed  Google Scholar 

  • Schreiner M, Beyene B, Krumbein A, Stützel H (2009) Ontogenetic changes of 2-propenyl and 3-indolylmethyl glucosinolates in Brassica carinata leaves as affected by water supply. J Agric Food Chem 57:7259–7263

    Article  CAS  PubMed  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    PubMed  Google Scholar 

  • Seca ML, Diana CG, Pinto A (2019) Biological potential and medical use of secondary metabolites. Medicines 6:66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seneviratne G, Jayasinghearachchi HS (2003) Mycelial colonization by bradyrhizobia and azorhizobia. J Biosci 28:243–247

    Article  PubMed  Google Scholar 

  • Seung KJ, Keshavjee S, Rich ML (2015) Multidrug-resistant tuberculosis and extensively drug-resistant tuberculosis. Cold Spring Harb Perspect Med 5:017863

    Article  Google Scholar 

  • Sgherri C, Stevanovic B, Navari IF (2004) Role of phenolics in the antioxidative status of the resurrection plant Ramondaserbica during dehydration and rehydration. Physiol Plant 122:478–88

    Article  CAS  Google Scholar 

  • Shabana YM, Abdel FGM, Ismail AE, Rashad YM (2008) Control of brown spot pathogen of rice (Bipolarisoryzae) using some phenolic antioxidants. Braz J Microbiol 39:438–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi H, Liu Z, Zhu L, Zhang C, Chen Y, Zhou Y, Li F, Li X (2012) Overexpression of cotton (Gossypium hirsutum) dirigent1 gene enhances lignification that blocks the spread of Verticillium. Acta Biochim Biophys Sin 44:555–564

    Article  CAS  PubMed  Google Scholar 

  • Singh PK, Singh R, Singh S (2013) Cinnamic acid induced changes in reactive oxygen species scavenging enzymes and protein profile in maize (Zea mays L) plants grown under salt stress. Physiol Mol Biol Plants 19:53–59

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Gupta R, Pandey R (2017) Exogenous application of rutin and gallic acid regulate antioxidants and alleviate reactive oxygen generation in Oryza sativa L. Physiol Plant Mol Biol 23:301

    Article  CAS  Google Scholar 

  • Singh RR, Chinnasri B, De Smet L, Haeck A, Demeestere K, Van Cutsem P, Van Aubel G, Gheysen G, Kyndt T (2019) Systemic defense activation by COS-OGA in rice against root-knot nematodes depends on stimulation of the phenylpropanoid pathway. Plant Physiol Biochem 142:202–210

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Avtar R, Pal A, Punia R, Singh VK, Bishnoi M, Singh A, Choudhary RR, Mandhania S (2020) Genotype-specific antioxidant responses and assessment of resistance against Sclerotinia sclerotiorum causing Sclerotinia rot in indian mustard. Pathogens 11:892

    Article  Google Scholar 

  • Skalicka WK, Orhan IE, Cordell GA, Nabavi SM, Budzyńska B (2016) Implication of coumarins towards central nervous system disorders. Pharmacol Res 103:188–203

    Article  Google Scholar 

  • Spencer DF, Ksander GG (1990) Influence of temperature, light and nutrient limitation on anthocyanin content of Potamogeton gramineus L. Aquatic Bot 38:357–367

    Article  CAS  Google Scholar 

  • Stella FTF, Stout MJ, SantAna J (2019) Effects of exogenous methyl jasmonate and salicylic acid on rice resistance to Oebalus pugnax. Pest Manag Sci 75:744–752

    Article  Google Scholar 

  • Sudheeran PK, Feygenberg O, Maurer D, Alkan N (2018) Improved cold tolerance of mango fruit with enhanced anthocyanin and flavonoid contents. Molecules 23:1832

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun F, Chen H (2007) Evaluation of enzymatic hydrolysis of wheat straw pretreated by atmospheric glycerol autocatalysis. J Chem Technol Biotechnol 82:1039–1044

    Article  CAS  Google Scholar 

  • Sun XF, Xu F (2005) Characteristics of degraded hemicellulosic polymers obtained from steam exploded wheat straw. Carbohyd Polym 60:15–26

    Article  CAS  Google Scholar 

  • Sun J, Qiu C, Ding Y, Wang Y, Sun L, Fan K, Gai Z, Dong G, Wang J, Li X, Song L (2020) Fulvic acid ameliorates drought stress-induced damage in tea plants by regulating the ascorbate metabolism and flavonoids biosynthesis. BMC Genom 21:1–13

    Article  Google Scholar 

  • Szabó B, Tyihák E, Szabó LG, Botz L (2003) Mycotoxin and drought stress induced change of alkaloid content of Papaver somniferum plantlets. Acta Bot Hung 45:409–417

    Article  Google Scholar 

  • Tak Y, Kumar M (2020) Phenolics: a key defence secondary metabolite to counter biotic stress. Plant phenolics in sustainable agriculture. Springer, pp 309–329

    Chapter  Google Scholar 

  • Tounekti T, Ahmedou V, Mustapha E, Habib K (2011) Ionic interactions and salinity affect monoterpene and phenolic diterpene composition in rosemary (Rosmarinus officinalis). J Plant Nutr Soil Sci 174:504–551

    Article  CAS  Google Scholar 

  • Tuladhar P, Sasidharan S, Saudagar P (2021) Role of phenols and polyphenols in plant defense response to biotic and abiotic stresses. In: Jogaiah S (ed) Biocontrol agents and secondary metabolites. Woodhead Publishing, pp 419–441

    Chapter  Google Scholar 

  • Turtola S, Manninen AM, Rikala R, Kainulainen P (2003) Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce seedlings. J Chem Ecol 29:1981–1995

    Article  CAS  PubMed  Google Scholar 

  • Tzin V, Rogachev I, Meir S, Moyal BZM, Masci T, Vainstein A (2015) Altered levels of aroma and volatiles by metabolic engineering of shikimate pathway genes in tomato fruits. AIMS Bioeng 2:75–92

    Article  CAS  Google Scholar 

  • Ullah C, Tsai CJ, Unsicker SB, Xue L, Reichelt M, Gershenzon J, Hammerbacher A (2018) Salicylic acid activates poplar defense against the biotrophic rust fungus Melampsoralarici-populina via increased biosynthesis of catechin and proanthocyanidins. New Phytol 221:960–975

    Article  PubMed  PubMed Central  Google Scholar 

  • Valentines MC, Vilaplana R, Torres R, Usall J, Larrigaudiere C (2005) Specific roles of enzymatic browning and lignification in apple disease resistance. Postharvest Biol Technol 36:227–234

    Article  CAS  Google Scholar 

  • Valifarda M, Mohsenzadeha S, Kholdebarina B, Rowshanb V (2014) Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. S Afr J Bot 93:92–97

    Article  Google Scholar 

  • Van B, Frank V, Eva DJ (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414

    Article  Google Scholar 

  • Vance CP, Kirk TK, Sherwood RT (2003) Lignification as a mechanism of disease resistance. Ann Rev Phytopathol 18:259–288

    Article  Google Scholar 

  • Vasconsuelo A, Boland R (2007) Molecular aspects of the early stages of elicitation of secondary metabolites in plants. Plant Sci 172:861–875

    Article  CAS  Google Scholar 

  • Verhoeyen ME, Bovy A, Collins G, Muir S, Robinson S, De Vos CHR, Colliver S (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53:2099–2106

    Article  CAS  PubMed  Google Scholar 

  • Verpoorte R, Memelink J (2002) Engineering secondary metabolite production in plants. Curr Opin Biotechnol 13:181–187

    Article  CAS  PubMed  Google Scholar 

  • Vuolo MM, Lima VS, Maróstica MR (2019) Junior phenolic compounds: Structure, classification, and antioxidant power. In: Campos MRS (ed) Bioactive compounds: health benefits and potential applications. Woodhead Publishing, pp 33–50

    Chapter  Google Scholar 

  • Wang DH, Du F, Liu HY, Liang ZS (2010) Drought stress increases iridoid glycosides biosynthesis in the roots of Scrophularia ningpoensis seedlings. J Med Plants Res 4:2691–2699

    Article  CAS  Google Scholar 

  • Wang Q, Cao K, Li H, Zhu G, Fang W, Chen C, Wang X, Wang L (2018) Lignification plays an important role on resistance to root-knot nematode (Meloidogyne incognita) based on contrastive analysis in peach. Sci Hortic 238:1–6

    Article  CAS  Google Scholar 

  • Wang F, Tan H, Huang L, Cai C, Ding Y, Bao H, Chen Z, Zhu C (2021) Application of exogenous salicylic acid reduces Cd toxicity and Cd accumulation in rice. Ecotoxicol Environ Saf 207:111198

    Article  CAS  PubMed  Google Scholar 

  • Wi SG, Cho EJ, Lee DS (2015) Lignocellulose conversion for biofuel: a new pretreatment greatly improves downstream biocatalytic hydrolysis of various lignocellulosic materials. Biotechnol Biofuels 8:228

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams RJ, Spencer JP, Rice-Evans C (2004) Flavonoids: antioxidants or signalling molecules. Free Rad Biol Med 36:838–849

    Article  CAS  PubMed  Google Scholar 

  • Wink M, Botschen F,Gosmann C, Schäfer H, Waterman PG (2010) Chemotaxonomyseen from a phylogenetic perspective and evolution of secondary metabolism.In: Wink, M. (Eds), Biochemistry of plant secondary metabolism. Afr J Bot 89:164–175

  • Winkel SB (2001) It takes a garden. How work on diverse plant species has contributed to an understanding of flavonoid metabolism. Plant Physiol 127:1399–1404

    Article  Google Scholar 

  • Winkel BSJ (2004) Metabolic channeling in plants. Ann Rev Plant Biol 55:85–107

    Article  CAS  Google Scholar 

  • Woo JW, Kim JK, Won SI, Corvalán C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, Kim JS et al (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33:1162–1164

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Lin L (2003) Enhancement of taxol production and release in Taxus chinensis cell cultures by ultrasound, methyl jasmonate and in situ solvent extraction. Appl Microbiol Biotechnol 62:151–155

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H et al (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genom Res 23:396–408

    Article  CAS  Google Scholar 

  • Wuyts N, Lognay G, Verscheure M, Marlier M, Waele DD, Swennen R (2007) Potential physical and chemical barriers to infection by the burrowing nematode Radopholussimilis in roots of susceptible and resistant banana (Musa spp.). Plant Pathol 56:878–890

    Article  CAS  Google Scholar 

  • Wyman CE, Dale BE, Elander RT, Holtzapple M, Ladisch MR, Lee YY, Saddler JN (2009) Comparative sugar recovery and fermentation data following pretreatment of poplar wood by leading technologies. Biotechnol Prog 25:333–339

    Article  CAS  PubMed  Google Scholar 

  • Xing B, Liang L, Liu L, Hou Z, Yang D, Yan K, Zhang X, Liang Z (2018) Overexpression of SmbHLH148 induced biosynthesis of tanshinones as well as phenolic acids in Salvia miltiorrhiza hairy roots. Plant Cell Rep 37:1681–1692

    Article  CAS  PubMed  Google Scholar 

  • Xuan TD, Khang DT (2018) Effects of exogenous application of protocatechuic acid and vanillic acid to chlorophylls, phenolics and antioxidant enzymes of rice (Oryza sativa L.) in submergence. Molecules 23:620

    Article  PubMed  PubMed Central  Google Scholar 

  • Yadu S, Dewangan TL, Chandrakar V, Keshavkant S (2017) Imperative roles of salicylic acid and nitric oxide in improving salinity tolerance in Pisum sativum L. Physiol Mol Biol Plants 23:43–58

    Article  CAS  PubMed  Google Scholar 

  • Yang CQ, Fang X, Wu XM, Mao YB, Wang LJ, Chen XY (2012) Transcriptional regulation of plant secondary metabolism. J Integ Plant Biol 54:703–712

    Article  CAS  Google Scholar 

  • Yao Q, Peng Z, Tong H, Yang F, Xing G, Wang L, Zheng J, Zhang Y, Su Q (2019) Tomato plant flavonoids increase whitefly resistance and reduce spread of tomato yellow leaf curl virus. J Econ Entomol 112:2790–2796

    CAS  PubMed  Google Scholar 

  • Yildiztugay E, Ozfidan KC, Kucukoduk M, Turkan I (2020) Flavonoid naringenin alleviates short-term osmotic and salinity stresses through regulating photosynthetic machinery and chloroplastic antioxidant metabolism in Phaseolus vulgaris. Front Plant Sci 11:682

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan Y, Liu Y, Wu C, Chen S, Wang Z, Yang Z, Qin S, Huang L (2012) Water deficit affected flavonoid accumulation by regulating hormone metabolism in Scutellaria baicalensis Georgi roots. PLoS ONE 7:42946

    Article  Google Scholar 

  • Yue W, Ming QL, Lin B, Rahman K, Zheng CJ, Han T, Qin LP (2016) Medicinal plant cell suspension cultures: Pharmaceutical applications and high-yielding strategies for the desired secondary metabolites. Crit Rev Biotechnol 36:215–232

    Article  CAS  PubMed  Google Scholar 

  • Zaid A, Mohammad F, Siddique KH (2022) Salicylic acid priming regulates stomatal conductance, trichome density and improves cadmium stress tolerance in Mentha arvensis L. Front Plant Sci 13:895427

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Subramanian S, Stacey G, Yu O (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant J 57:171–183

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Butelli E, De Stefano R, Schoonbeek HJ, Magusin A, Pagliarani C, Wellner N, Hill L, Orzaez D, Granell A et al (2013) Anthocyanins double the shelf life of tomatoes by delaying overripening and reducing susceptibility to gray mold. Curr Biol 23:1094–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Wu L, Wang X, Chen B, ZhaoJ CJ, Li Z, Yang J, Wu L, Wu ZG (2019) The cotton laccase gene GhLAC15 enhances Verticillium wilt resistance via an increase in defence-induced lignification and lignin components in the cell walls of plants. Mol Plant Pathol 20:309–322

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Martinelli E, Senizza B, Miras MB, Yildiztugay E, Arikan B, Elbasan F, Ak G, Balci M, Zengin G, Rouphael Y (2021) The Combination of mild salinity conditions and exogenously applied phenolics modulates functional traits in lettuce. Plants 10:1457

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhu WH, Hu Q (2001) Selection of fungal elicitors to increase indole alkaloid accumulation in Catharanthus roseus suspension cell culture. Enzym MicrobTechnol 28:666–672

    Article  CAS  Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Jia X, Wang W, Liu T, Huang S, Yang M (2016) Growth under elevated air temperature alters secondary metabolites in Robiniapseudoacacia L. seedlings in Cd and Pb-contaminated soils. Sci Total Environ 565:586–594

    Article  CAS  PubMed  Google Scholar 

  • Zhi S, Liu Y, Yu X, Wang X, Lu X (2012) Enzymatic hydrolysis of cellulose after pretreated by ionic liquids: focus on one-pot process. Energy Procedia 14:1741–1747

    Article  Google Scholar 

  • Zu YG, Tang ZH, Yu JH, Liu SG, Wang W, Guo XR (2003) Different responses of camptothecin and 10-hydroxycamptothecin to heat shock in Camptotheca acuminata seedlings. J Integ Plant Biol 45:809–814

    CAS  Google Scholar 

  • Zulfiqar F, Ashraf M (2021a) Bioregulators: unlocking their potential role in regulation of the plant oxidative defense system. Plant Mol Biol 105:11–41

    Article  CAS  PubMed  Google Scholar 

  • Zulfiqar F, Ashraf M (2021b) Nanoparticles potentially mediate salt stress tolerance in plants. Plant Physiol Biochem 160:257–268

    Article  CAS  PubMed  Google Scholar 

  • Zulfiqar F, Akram NA, Ashraf M (2020) Osmoprotection in plants under abiotic stresses: new insights into a classical phenomenon. Planta 251:1–17

    Article  Google Scholar 

  • Zykin PA, Andreeva EA, Lykholay AN, Tsvetkova NV, Voylokov AV (2018) Anthocyanin composition and content in rye plants with different grain color. Molecules 23:948

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

Not applicable.

Author information

Authors and Affiliations

  1. Department of Horticultural Sciences, University of Florida, Gainesville, FL, 32611, USA

    Yogesh K. Ahlawat

  2. College of Agriculture CCS HAU, Hisar, India

    Manjeet Singh

  3. Molecular Biology and Biotechnology Department, CCS HAU, Hisar, India

    K. Manorama & Nita Lakra

  4. Department of Botany, Govt. Gandhi Memorial Science College, Cluster University, Canal Road 180001, Jammu, Jammu and Kashmir, India

    Abbu Zaid

  5. Plant Physiology and Biochemistry Section, Department of Botany, Aligarh Muslim University, Aligarh, India

    Abbu Zaid

  6. Department of Horticultural Sciences, Faculty of Agriculture and Environment, The Islamia University of Bahawalpur, Bahawalpur, 63100, Pakistan

    Faisal Zulfiqar

Authors
  1. Yogesh K. Ahlawat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manjeet Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Manorama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nita Lakra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abbu Zaid
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Faisal Zulfiqar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YKA, AZ, and MM wrote the manuscript. NL, AZ, and FZ planned the structure of the draft and are also actively involved in the critical reviewing of the manuscript.

Corresponding authors

Correspondence to Yogesh K. Ahlawat, Nita Lakra or Abbu Zaid.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Informed consent statement

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahlawat, Y.K., Singh, M., Manorama, K. et al. Plant phenolics: neglected secondary metabolites in plant stress tolerance. Braz. J. Bot (2023). https://doi.org/10.1007/s40415-023-00949-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s40415-023-00949-x

Keywords

Search

Navigation